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Contents lists available at SciVerse ScienceDirect

Aquatic Botany

journa l homepage: www.elsevier.com/locate/aquabot

A persistent bloom of J.V. Lamouroux (,

Chlorophyta) in Biscayne Bay, Florida

a,b,∗ c c d

Ligia Collado-Vides , Christian Avila , Stephen Blair , Frederik Leliaert ,

e f a a

Dení Rodriguez , Travis Thyberg , Sabrina Schneider , Janina Rojas ,

g f f

Pamela Sweeney , Crawford Drury , Diego Lirman

a

Department of Biological Sciences, OE 167, Florida International University, Miami, FL 33199, USA

b

Southeast Environmental Research Center, Florida International University, Miami, FL 33199, USA

c

Natural Resource Division, Department of Regulatory and Economic Resources-Environmental Resources Management, 701 NW 1st Court, Miami, FL

33136, USA

d

Phycology Research Group, Biology Department, Ghent University, Krijgslaan 281 S8, 9000 Ghent, Belgium

e

Laboratorio de Ficología, Departamento de Biología Comparada, Facultad de Ciencias, Univerisdad Nacional Autónoma de México, D.F. 04510, Mexico

f

University of Miami, Rosenstiel School of Marine and Atmospheric Science, 4600 Rickenbacker Causeway, Miami, FL 33149, USA

g

Department of Environmental Protection, 1277 NE 79 Street, Miami, FL 33138, USA

a

r t a b

i c l e i n f o s t r a c t

Article history: Green macroalgal blooms are becoming a common problem in coastal waters and estuaries. This study

Received 25 October 2012

describes the first occurrence of a persistent macroalgal bloom of the genus Anadyomene J.V. Lam-

Received in revised form 10 June 2013

ouroux (, Anadyomenaceae) in the world and particularly in Biscayne Bay, FL, USA. The

Accepted 12 June 2013

morphological-based identification of species was verified by a molecular analysis that sequenced the

Available online xxx

variable C1D2 region of the large subunit (LSU) nrDNA. Results indicate that the bloom is composed of

two species: Anadyomene stellata, reported previously for Florida, and a diminutive perforate undeter-

Keywords:

mined species, Anadyomene sp., potentially representing an introduction in the area. General surveys in

Harmful algal bloom

Anadyomene Biscayne Bay based on a stratified random design, to visually estimate the percent cover of submerged

aquatic vegetation, date from 1999; using the same methods recent intensive surveys of the detected

Biscayne Bay

Siphonocladales bloom were conducted once a year from 2010 to 2012. Results show that the Anadyomene bloom densities

2

South Florida have persisted since 2005 through 2012 covering an area of approximately 60 km of seagrass habitats.

Ulvophyceae The spatial distribution of the bloom is restricted to the central inshore section of the Bay, an area affected

by canals and groundwater discharges. The persistent 75% cover reported for several sites, has caused

significant negative impacts to seagrass beds. This bloom occurring adjacent to metropolitan Miami, adds

to the world trend of increasing green macroalgal blooms occurring at enriched coastal waters. © 2013 Elsevier B.V. All rights reserved.

1. Introduction

Harmful algal blooms (HAB) are becoming an increasingly sig-

nificant problem as population and coastal development continue

to grow (Ye et al., 2011). The problem is so prevalent that almost

every country with a coastline has either experienced a bloom or

∗

Corresponding author at: Department of Biological Sciences, OE 167, Florida

is facing the risk of one (Anderson, 2009). Algal blooms are gener-

International University, Miami, FL 33199, USA. Tel.: +1 305 348 2274;

ally associated with phytoplankton (microalgae and cyanobacteria)

fax: +1 305 348 1986.

species, however, several macroalgal species are also known to

E-mail addresses: colladol@fiu.edu, [email protected]

(L. Collado-Vides), [email protected] (C. Avila), [email protected] bloom (Valiela et al., 1997; Smith et al., 2005; Pinón-Gimate˜ et al.,

(S. Blair), [email protected] (F. Leliaert),

2009; Nelson et al., 2008). These ephemeral or persistent HABs

[email protected] (D. Rodriguez), [email protected]

have been associated with nutrient loads from urban or agricul-

(T. Thyberg), sschn002@fiu.edu (S. Schneider), jroja020@fiu.edu (J. Rojas),

tural drainages and other sources such as shrimp farms (Valiela

[email protected].fl.us (P. Sweeney), [email protected] (C. Drury),

[email protected] (D. Lirman). et al., 1997; Pinón-Gimate˜ et al., 2009). Introduced algal species

0304-3770/$ – see front matter © 2013 Elsevier B.V. All rights reserved.

http://dx.doi.org/10.1016/j.aquabot.2013.06.010

Please cite this article in press as: Collado-Vides, L., et al., A persistent bloom of Anadyomene J.V. Lamouroux (Anadyomenaceae, ) in

Biscayne Bay, Florida. Aquat. Bot. (2013), http://dx.doi.org/10.1016/j.aquabot.2013.06.010

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have been also associated with blooms, such as Caulerpa taxifolia

(M. Vahl) C. Agardh in the Mediterranean or Caulerpa brachypus f.

parvifolia (Harvey) A.B. Cribb in Florida, making the identification of

any algal bloom species a very important step for its management

(William and Smith, 2007; Lapointe and Bedford, 2010; Guidone

and Thornber, 2013).

Macroalgal blooms have been reported to be composed of red,

green and brown algae (Valiela et al., 1997; William and Smith,

2007); however the majority and largest blooms are found within

species of the Chlorophyta phylum. Some “green tides” reported

belong to the , including several species of the gen-

era Ulva Linnaeus and Monostroma Thuret. The largest macroalgal

bloom reported so far is the Ulva prolifera O.F. Müller 2008 bloom

offshore of Qingdao, China. This bloom which span was approxi-

2

mately 13,000 km in the Yellow Sea produced approximately 20

million wet tons of algae with an extremely expensive manage-

ment cost (Leliaert et al., 2009; Liu et al., 2009). Other examples of

blooming-forming species of the class Ulvophyceae include tem-

perate species such as Cladophora vagabunda (Linnaeus) Hoek in

Waquoit Bay, MA, USA (Peckol et al., 1994); and tropical species

such as Cladophora prolifera (Roth) Kützing in Bermuda which

lasted for several decades (Bach and Josselyn, 1978; Lapointe and

O’Connell, 1989). Recent reports include Anadyomene gigantodyc-

tion Littler and Littler, found overgrowing deep water gorgonian

corals in Belize (Littler and Littler, 2012) and Boodlea composite

(Harvey) F. Brand at the Northwester Hawaiian Islands (Vroom

et al., 2009). All the above mentioned species have in common

a morphology and anatomy that results in a high surface area

to volume ratio (SA:V) that suggests they can respond rapidly to

increased nutrient inputs (Littler and Littler, 1980).

Biscayne Bay is a subtropical estuarine lagoon within Miami-

Dade County, FL, and adjacent to the City of Miami, which has

approximately 450,000 inhabitants, with 2.5 million inhabitants

in the county. Since early 1950s, the hydrology of the bay has

Fig. 1. Map of Biscayne Bay showing the distribution of the algal bloom. (a) General

been altered to meet the needs of the growing population and geographical location of the bloom, (b) zoom of the bloom abundance distribution.

has become subject to dredging, urban runoff, sewage, and other

anthropogenic influences that have altered the health and function

and call the attention to shifting conditions in coastal waters with

of the ecosystem (Light and Dineen, 1994). In addition, the port of

potential negative consequences on the structure and function of

Miami, located in Biscayne Bay, has a large cargo and tourism traffic

seagrass habitats.

increasing the likelihood of species introduction in the area.

The submerged aquatic vegetation (SAV) of the lagoon is charac-

terized by seagrasses and drifting and rhizophytic macroalgae, with 2. Methods

approximately 60 species reported; including one species of Anady-

omene (Biber and Irlandi, 2006; Lirman et al., 2008; Collado-Vides 2.1. Study area

et al., 2011). Biscayne Bay has the lowest water column nutrient

concentrations in the state, however, specific regions of Biscayne Biscayne Bay is adjacent to the city of Miami, FL, USA

◦ ◦

Bay are reported to have higher water-column nutrients indica- (25 33 57 N, 80 12 59 W) (Fig. 1). Due to its natural and economic

tive of terrestrial/groundwater nutrient loading (Caccia and Boyer, importance, Biscayne Bay is designated an Outstanding Florida

2007; Stalker et al., 2009). These conditions are consistent with Waterway by the state of Florida. Biscayne Bay is comprised of

the high nitrogen (N) content found in seaweed tissue reported two state aquatic preserves and a national park. Biscayne National

by Collado-Vides et al. (2011), which are similar to/or higher than Park is located in the central part of the bay and is managed by

those found in algae under experimentally enriched treatments, the National Park Service. The Biscayne Bay Aquatic Preserves are

as well as those growing close to nutrient-rich mangrove areas located to the north and south of the national park, where the bloom

(Lapointe, 1987, 1997), suggesting that SAV organisms are growing is most dense, and is managed by the Florida Department of Envi-

exposed to relatively high nutrient availability indicating elevated ronmental Protection. The lagoon is a coastal estuary affected by

risk levels for blooming events. freshwater and nutrient inputs from canals, groundwater, precip-

Consistent with these nutrient patterns, we report the first itation, and overland flows (Caccia and Boyer, 2007; Stalker et al.,

occurrence of a persistent bloom of Anadyomene V.J. Lamouroux 2009). The submerged aquatic vegetation of Biscayne Bay is char-

(Cladophorales, Anadyomenaceae) species. Morphological and acterized by four seagrass species with the dominance of Thalassia

phylogenetic molecular analyses were used to test the taxonomic testudinum Banks ex König, followed by Halodule wrightii Ascher-

identity of the blooming species, which has the potential of being son, and Syringodium filiforme Kützing. Ruppia maritima Linnaeus

a new record for the study site. Due to the presence of canals, the has a limited presence, reduced to areas with high fresh water

highest abundance and persistence of the bloom is expected to be loads. Approximately 60 species of macroalgae have been reported

close to areas affected by canals discharges compared with areas within Biscayne Bay, with a dominance of species in the genera Hal-

further offshore. The information included in this study adds to imeda J.V. Lamouroux and Penicillus Lamarck within seagrass beds

the increasing list of green macroalgal blooms in coastal habitats, under marine conditions, and red algae of the genus Laurencia J.V.

Please cite this article in press as: Collado-Vides, L., et al., A persistent bloom of Anadyomene J.V. Lamouroux (Anadyomenaceae, Chlorophyta) in

Biscayne Bay, Florida. Aquat. Bot. (2013), http://dx.doi.org/10.1016/j.aquabot.2013.06.010

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Lamouroux within seagrasses exposed to lower and more variable normality and homogeneity of variance (Underwood, 1997). A mul-

salinity (Collado-Vides et al., 2011). The bottom where the bloom tiple ANOVA followed by a post hoc Bonferroni multiple comparison

was found is dominated by T. testudinum and algae of the genus test was applied to detect changes on species abundance, through

Halimeda and Penicillus. time and space for all data from 2010 through 2012, with time

(years), groups (close to canal, central, north, south edge and cen-

2.2. Morphological identification tral edge) and time*group as factors. A one-way ANOVA was applied

for each area (groups) with year as a factor to detect area-specific

Algal material was collected at the bloom sites, and preserved changes through time. A Pearson correlation was applied to all per-

in 4% formaldehyde seawater solution for identification. Taxonomic cent cover data to evaluate relationships between Anadyomene sp.

characteristics were evaluated following Littler and Littler (1991). and T. testudinum. All statistical analyses were conducted in SPSS v.

Live material was collected, and rapidly dried in 20 ml vials with 19.

silica gel for molecular analysis; some live material was kept fresh

and used to measure cell dimensions and take photographs. Micro- 3. Results

scopic pictures were taken with an eye piece camera ScopeTech

(Hangzhou, China), using a Leica microscope. Measurements were Two species were observed forming the bloom; one species

made with a calibrated ocular micrometer. is a sturdy eperforate blade form, while the second species is a

diminutive perforate form. The bloom was found in shallow waters

2.3. Molecular phylogeny between 2 and 4 m deep, and specimens were usually observed

drifting or entangled on seagrass (Fig. 2a).

Morphology-based species identification was verified by

sequencing the variable C1D2 region of the large subunit (LSU) 3.1. Morphological analysis

nrDNA of two Anadyomene specimens from the blooming area

in Biscayne Bay, in addition to seven additional specimens The diminutive form of Anadyomene covered large areas of sea-

of Anadyomene pavonina from Panama, and A. stellata from grass beds and, in some sites, completely overgrew the seagrass

Panama, Costa Rica, and Greece. DNA extraction, polymerase shoots (Fig. 2b, Fig. A1). This species has a foliose, highly per-

chain reaction (PCR) amplification and sequencing were per- forate mesh-like, and decumbent thallus, up to 5 cm in length

formed as described in Leliaert et al. (2007a). The newly generated and 3 cm wide. Veins are composed of uniseriate chains of cylin-

sequences are deposited in EMBL/GenBank under accession num- drical cells, decreasing in length distally; proximal vein cell

bers HF936684–HF936692. These sequences were then combined dimensions are highly variable with cell length 0.66–1.1 mm,

with available sequences from the Anadyomene/Microdictyon clade cell width 0.13–0.23 mm, and cell length/width (l/w) ratio 3–8;

(Leliaert et al., 2007b), and aligned using MUSCLE (Edgar, 2004). mid-blade vein cell dimensions are less variable with cell length

Selection of the model of nucleotide substitution was performed 0.65–0.97 mm, cell width 0.13–0.19 mm width, and cell l/w ratio

using the Akaike information criterion with jModelTest v0.1.1 3.8–7; distal vein cell dimension are smaller with cell length

(Posada, 2008). Maximum likelihood (ML) phylogenetic analysis 0.32–0.57 mm, cell width 0.11–0.18 mm, and cell l/w ratio 2.1–3.5;

was performed using PhyML under a general time-reversible model veins branch polychotomously with 3–6 branches radiating periph-

with gamma distribution split into four categories and no separate erally throughout the blade. Interstitial cells are ovoid or elliptical,

rate class for invariable sites (GTR + G). The reliability of internal arranged randomly and branching polychotomously; little or no

branches was evaluated with nonparametric bootstrapping (1000 overlap of adjacent cells throughout the blade, blunt attachment of

replicates). The tree was rooted with “Boodlea” vanbosseae follow- interstitial cells with adjacent cells that lack tentacula. Most spec-

ing Leliaert et al. (2007b). imens unattached, with no clear stipe formed from descending

rhizoids, but rhizoidal elongations are present. The distal margin

2.4. Field surveys has terminal marginal cells that can be free or anastomosing to

adjacent cells. Our specimens lack distinct veins bordering perfora-

2.4.1. History and abundance tions. The morphological characteristics do not fit completely with

Benthic habitats of Biscayne Bay have been monitored for more any described species therefore we leave it as undetermined.

than 3 decades by Miami-Dade County. Systematic monitoring The larger Anadyomene form was also found covering large

cover started in 1999 and 2003, by Miami Dade County and the extensions of seagrass beds (Fig. 2c, Fig. A2). It had an erect foliose

University of Miami, respectively, conducting surveys based on a thallus, up to 8 cm tall, and grew as sturdy fronds forming dense

stratified random design, to visually estimate the percent cover clumps; blades were eperforate and robust. Veins are composed

of SAV. The percent cover of seagrass and green macroalgae was of single uniseriate chains, with cylindrical cells slightly swollen

2

estimated for each site using in situ 0.25 m quadrats (Miami at their distal ends. The veins decrease in size toward distal mar-

Dade County, n = 4 quadrats per site) or photographs (University gin; proximal veins cell length 1–1.8 mm, cell width 0.14–0.27 mm,

of Miami, 10 images per site) (Lirman et al., 2008). Starting in 2010, cell l/w ratio 5.4–11.2; mid-blade cell length 0.68–1.15 mm, cell

an intensive monitoring program was concentrated on the area of width 0.12–0.22 mm, cell l/w ratio 3.8–8.1, distal cell length

Biscayne Bay where the algal bloom was dominant. These targeted 0.38–0.98 mm, cell width 0.13–0.21, cell l/w ratio 2.7–4.6; intersti-

2

surveys covered approximately 70 km (Fig. 1), a total of 181 sites tial cells generally arranged parallel to each other; rhizoids mainly

were surveyed in 2010–2012. Sites were aggregated in five groups in the basal regions of blades; veins polychotomously branching

based on geographic characteristics, group 1 included all sites in (2–6 branches); growing edge smooth or lobed, composed of small

proximity to canal areas, group 2 included sites in the central part round or oval cells. The morphological characteristics of these spec-

of the bloom, group 3 clumped sites at the edge of bloom on the imens fit the description of Anadyomene stellata (Wulfen) C. Agardh.

central area, group 4 contained the sites at the south edge of the

bloom and group 5 clumped sites in the north area of the bloom. 3.2. Molecular analysis

2.4.2. Statistical analysis The partial large subunit (LSU) rDNA alignment, containing 41

The 2010–2012 surveys resulted in a very large data-set, robust sequences of the Anadyomene/Microdictyon clade was 630 sites

enough to apply parametric tests even if they do not comply with long, including 56 variable sites. The maximum likelihood tree is

Please cite this article in press as: Collado-Vides, L., et al., A persistent bloom of Anadyomene J.V. Lamouroux (Anadyomenaceae, Chlorophyta) in

Biscayne Bay, Florida. Aquat. Bot. (2013), http://dx.doi.org/10.1016/j.aquabot.2013.06.010

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Table 1

Two-Way ANOVA for all 2010–2012 data, group, year and group*year as factors. Asp,

Anadyomene sp.; As, Anadyomene stellata; Hw, Halodule wrightii; Sf, Syringodium fili-

forme; Tt, Thalassia testudinum. Superscript numbers by species represent Bonferroni

significant differences.

Factor Species df Mean square F p

3-4

Asp 4 83337.856 85.009 <0.0001

1-2-3-4

As 4 4338.549 20.280 <0.0001

3

Group Hw 4 560.864 18.314 <0.0001

3

Sf 4 1111.033 7.383 <0.0001 3-4-5

Tt 4 15889.045 22.088 <0.0001

1-3

Asp 2 23464.859 23.935 <0.0001

1-2

As 2 689.967 3.225 0.040

Year Hw 2 52.430 1.712 0.181

2-3

Sf 2 144.960 0.963 0.382 1-2-3

Tt 2 6896.595 9.587 <0.0001

Asp 8 6372.463 6.500 <0.0001

As 8 458.007 2.141 0.030

Group*year Hw 8 161.294 5.267 <0.0001

Sf 8 90.027 0.598 0.780

Tt 8 2303.524 3.202 0.001

3.3. Bloom abundance spatial and temporal distribution

The dominant SAV species observed in the region of the algal

bloom within Biscayne Bay were T. testudinum (average cover of

26%), followed by S. filiforme (average cover of 4%), and H. wrightii

(average cover of 1%). Macroalgal species were rare and repre-

sented by species of the genus Halimeda and Penicillus, occasional

drifting red masses composed by species of the Laurencia complex

could be found in areas boarding the bloom region. The overall area

was dominated by the two blooming Anadyomene species; with an

overall average cover of 42%.

Anadyomene species have been detected in low abundance

within the Bay since the beginning of the surveys (1999), and

the majority of the sites surveyed during the following years

(1999–2004) had a % cover between 0% and 50%. Very few sites

showing a % cover >50%. The opposite pattern was detected for

the dominant seagrass, T. testudinum, which had in many sites

a % cover >75% during the 1999–2004 period. During the years

of 2005–2008 the Anadyomene bloom was concentrated at the

north-central inshore section of the Bay, covering an area of approx-

2

imately 60 km . In that same period the abundance of the bloom

increased considerably reaching 100% cover in several sites (Fig. 4).

The cover of Anadyomene sp. and T. testudinum showed an inverse

relationship over time, where the cover of T. testudinum was high

in the period between 1999 and 2004, but decreased significantly

between 2005 and 2008. Conversely, the abundance of Anadyomene

sp. was low during 1999–2004, and increased significantly during

2005–2008.

The intensive three year surveys in the bloom area showed

that the overall abundance of the three seagrasses and the two

Anadyomene species had a characteristic spatial distribution with

significant differences between areas. Anadyomene sp. had the

Fig. 2. (a) blooming area reaching 100% cover displacing seagrass, (b) Anadyomene

highest abundances close to canals, in the center of the bloom and

sp. habit, (c) A. stellata habit.

in the north area, while, A. stellata was concentrated at the north of

the bloom. T. testudinum was abundant at the edges of the bloom,

while S. filiforme and H. wrightii had an insignificant presence at the

central edge of the bloom, with minimal abundance in the rest of

shown in Fig. 3. The sequence data showed that the two specimens

the study area (Fig. 5, Table 1).

from the bloom belong to two different species. One sequence clus-

Overall abundance of Anadyomene sp., and T. testudinum had

ters with specimens identified as A. stellata from the Mediterranean

significant variability through time (Fig. 6, Table 1). A significant

Sea, Canary Islands and the Caribbean Sea. A. stellata was sister to

decrease of abundance was detected for Anadyomene sp. from

Anadyomene saldanhae Joly et Oliveira Filho also including speci-

2011 to 2012 (Table 1) and an increase of T. testudinum by 2012.

mens from both sides of the Atlantic Ocean. The other specimen,

No significant differences between years were found for S. filiforme

morphologically undetermined, formed a singleton that was most

and H. wrightii abundance (Table 1); however the variability in

closely related to the A. stellata–A. saldanhae clade.

abundance was different per area (Fig. 7, Table 2). The area close

Please cite this article in press as: Collado-Vides, L., et al., A persistent bloom of Anadyomene J.V. Lamouroux (Anadyomenaceae, Chlorophyta) in

Biscayne Bay, Florida. Aquat. Bot. (2013), http://dx.doi.org/10.1016/j.aquabot.2013.06.010

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Fig. 3. Maximum likelihood tree of the Anadyomene/Microdictyon clade inferred from partial LSU nrDNA sequences, showing the phylogenetic position of Anadyomene stellata

and Anadyomene sp. from Florida. ML bootstrap values (>50) are indicated at branches.

to canals had the highest variability, with four species showing with confirmed DNA records from the Mediterranean Sea (type

significant variation in cover over the period between 2010 and locality), Canary Islands and the Caribbean Sea. Another specimen,

2012. The Central and Central Edge portions were apparently less previously identified as A. stellata from the Philippines (Leliaert

dynamic with 2 species showing significant variation over time, et al., 2003), clearly belongs to a different species. A. stellata is

and the South Edge and North Area were least dynamic, with only closely related to A. saldanhae, which also has an amphi-Atlantic

Anadyomene sp. showing significant variation over time. distribution, and Anadyomene sp. is sister to that clade. As in

previously published LSU-based phylogenies, the monophyly of

4. Discussion Anadyomene and Microdictyon was not supported (Leliaert et al.,

2007a,b). With the provided morphological and molecular anal-

The persistent green macroalgal bloom in Biscayne Bay, Florida, ysis, the identification of A. stellata is clear and robust. A. stellata

is composed of two Anadyomene species. Thirteen Anadyomene has previously been reported for Florida (Littler and Littler, 2000;

species are described worldwide, from those, nine species are Dawes and Mathieson, 2008) and particularly to Biscayne Bay

present in the tropical Western Atlantic coasts, 6 have an eperfo- (Collado-Vides et al., 2011). However, this is the first report for

rated blade while only 3 have mesh-like thallus with perforated this species reaching blooming characteristics.

blade (Alves et al., 2011; Littler and Littler, 2012). The morpholog- Anadyomene sp. is a perforated species morphologically clearly

ical identification of A. stellata from Biscayne Bay, confirmed based separated from two perforated species reported for the West-

on available DNA sequences has an amphi-Atlantic distribution ern Atlantic: Anadyomene gigantiodictyon Littler and Littler and

Please cite this article in press as: Collado-Vides, L., et al., A persistent bloom of Anadyomene J.V. Lamouroux (Anadyomenaceae, Chlorophyta) in

Biscayne Bay, Florida. Aquat. Bot. (2013), http://dx.doi.org/10.1016/j.aquabot.2013.06.010

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Fig. 5. Overall average % cover of species per area. Asp, Anadyomene sp.; As,

Anadyomene stellata; Hw, Halodule wrightii; Sf, Syringodium filiforme; Tt, Thalassia

testudinum.

although small rhizoids were detected. The absence of stipes can

be attributed to the drifting habit acquired during blooming stage,

it is well documented that drifting algae can modify some of their

morphological characteristics when losing their attachment to sub-

strate including the loss of their holdfast (Norton and Mathieson,

1983). A second difference is the absence of vein-encircled perfora-

tion described for mature specimens, which is likely a consequence

Fig. 4. Abundance of species on site revisited at different time intervals.

of the fact that the bloom-forming specimens were drifting

specimens in rapid blooming growth maintaining juvenile charac-

A. pavonina, (J. Agardh) Wille, the molecular data further con- teristics. These morphological inconsistencies and the lack of DNA

firmed that Anadyomene sp. is distinct from A. pavonina; at present data from the original A. linkiana do not allow us to completely iden-

DNA sequence data is lacking for the other perforate species, A. tify our material with this taxon. Further investigations are needed

gigantiodictyon. The morphological characteristics, such as cell size to confirm the identity of Anadyomene sp. as A. linkiana; or as a new

and general cell and branching patterns of our specimens closely species, in either case it will be a new record for Florida.

resemble the third eperforate described species for the Western Several cases have been reported in coastal ecosystems where

Atlantic Anadyomene linkiana Littler and Littler a diminutive perfo- nutrient enrichment can degrade an ecosystem functioning; exam-

rated species reported for deep waters of the Bahamas (Littler and ples are from freshwater and estuarine environments (Scheffer

Littler, 1991), however some distinct morphological characteristics and van Nes, 2007; Frankovich et al., 2011) and seagrass beds

were absent in our material. The original description of A. linkiana (McGlathery, 2001; Williams, 2007). Increased nutrient loadings in

mentions the presence of diminutive stipe formed by 3–9 rhi- coastal waters have been associated with a shift in dominance from

zoidal elongations. In our specimens, distinct stipes were lacking, seagrass and perennial macroalgae to ephemeral, bloom-forming

Fig. 6. Overall temporal abundance of species. Asp, Anadyomene sp.; As, Anadyomene stellata; Hw, Halodule wrightii; Sf, Syringodium filiforme; Tt, Thalassia testudinum.

Please cite this article in press as: Collado-Vides, L., et al., A persistent bloom of Anadyomene J.V. Lamouroux (Anadyomenaceae, Chlorophyta) in

Biscayne Bay, Florida. Aquat. Bot. (2013), http://dx.doi.org/10.1016/j.aquabot.2013.06.010

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L. Collado-Vides et al. / Aquatic Botany xxx (2013) xxx–xxx 7

Table 2

One-way ANOVA per area with year as factor. Asp, Anadyomene sp.; As, Anadyomene stellata; Hw, Halodule wrightii; Sf, Syringodium filiforme; Tt, Thalassia testudinum. Only

significant differences are presented.

Species Sum of squares df Mean square F p

Area 1: Close to canal

Asp 41332.019 2 20666.010 14.603 <0.0001

As 196.884 2 98.442 4.065 0.018

Tt 25603.297 2 12801.648 18.736 <0.0001

Hw 39.022 2 19.511 3.666 0.027

Area 2: Central area of the bloom

Asp 32526.717 2 16263.358 14.403 <0.0001

Tt 10309.844 2 5154.922 8.320 <0.0001

Area 3: Central edge

Tt 9392.446 2 4696.223 4.980 0.008

Hw 1508.585 2 754.293 8.491 <0.0001

Area 4: South Edge

Asp 3053.225 2 1526.613 3.164 0.049

Area 5: North area

Asp 28273.691 2 14136.845 11.153 <0.0001

algae (Anderson, 2009; Ye et al., 2011), a problem also observed the central area needs to be further examined (Stalker et al., 2009).

in coral reefs affected by ephemeral algal blooms (Smith et al., The temporal and spatial dynamics found showed that historically,

2005). Nevertheless not all species develop into large blooms, the the establishment of the bloom resulted in a detrimental effect

simple morphology of Anadyomene species with very high SA:V on the seagrasses; furthermore the significant temporal and spa-

is similar to other green blooming macroalgae known to incor- tial differences across areas might reflect the dynamics of nutrient

porate nutrients rapidly (Littler and Littler, 1980). For example sources and hydrological characteristics of the area (Stalker et al.,

Ulva Linnaeus in Finland (Blomster et al., 2002), Cladophora glom- 2009).

erata (Linnaeus) Kützing in the Baltic Sea (Gubelit and Berezina, Biscayne Bay is a fragile ecosystem at the edge of a densely

2010), Cladophora sericea (Hudson) Kützing in Denmark (Thybo- populated and highly developed area, as well as a large port sup-

Christesen et al., 1993), all simple single cell layers, or uniseriate porting high volumes of freight shipping and passenger ships. The

branching algae, have developed green algal blooms all around the presence of a bloom of a morphological simple species, including

coastal waters of the planet (see Ye et al., 2011 for a review). a new record for the area, might be a symptom of nutrient enrich-

Our extensive surveys indicate that, so far, the bloom of these ment that facilitates the expansion of seaweeds. The blooming

two thin green macroalgal species is limited to the north-central, species completely covered extensive areas of pre-existing seagrass

inshore areas of the bay. This distribution coincides with a region bed, resulting in the loss of significant coverage of seagrasses. The

characterized by Briceno˜ et al. (2011) as enriched by nutrients com- impacts to the seagrass habitats in Biscayne Bay can have dramatic

ing from canal discharges likely facilitating the rapid growth of effects in the ecosystem as demonstrated in other shallow water

fast growing algal species, as documented here where the highest seagrass environments (Williams, 2007; Nelson et al., 2008).

abundance of Anadyomene sp. was found close to areas affected by

canal discharges. Additionally the geology/hydrology of southeast

5. Conclusions

Florida, and Biscayne Bay, has been document to support significant

groundwater discharge to the bay (Langevin, 2003). The part that

In this study we reported an Anadyomene species complex per-

groundwater discharge may play in the persistence of the bloom in

sistent bloom in Biscayne Bay, Florida, which might be an important

sign of nutrient loadings in the Bay. This bloom is composed by A.

stellata, and Anadyomene sp., two green macroalgae, adding two

species to the list of green bloom forming macroalgae (Ye et al.,

2011; Williams, 2007). In the case of Anadyomene sp. this report

highlights the potential introduction of a new species blooming

once is present in rich waters, a possible phenomenon that we

might experience more frequently in coastal areas. The spatial

and temporal distribution of the blooming species is related with

areas affected by land nutrient sources such as canals, and possibly

groundwater discharges.

Acknowledgments

Authors are grateful to the editor, Dr. E. Gross and two anony-

mous reviewers that helped improve the manuscript. We want

to recognize the invaluable work of Gallia Varona, Kathryn Wil-

son, and Damaso Rosales for their field support. Field work was

supported by the Florida Department of Environmental Protection

Biscayne Bay Aquatic Preserve (A3927F and A57A9F contracts), the

Fig. 7. Cumulative abundance of species per area and year. Asp, Anadyomene sp.;

Natural Resource Division, Department of Regulatory and Economic

As, Anadyomene stellata; Hw, Halodule wrightii; Sf, Syringodium filiforme; Tt, Thalassia

testudinum. Resources-Environmental Resources Management, and the MAP

Please cite this article in press as: Collado-Vides, L., et al., A persistent bloom of Anadyomene J.V. Lamouroux (Anadyomenaceae, Chlorophyta) in

Biscayne Bay, Florida. Aquat. Bot. (2013), http://dx.doi.org/10.1016/j.aquabot.2013.06.010

G Model

AQBOT-2590; No. of Pages 9 ARTICLE IN PRESS

8 L. Collado-Vides et al. / Aquatic Botany xxx (2013) xxx–xxx

Fig. A.1. Anadyomene sp. morphological characteristics. (a) Thallus habit; (b) view of deumbent perforated mesh, arrows sign uniseriate proximal veins; (c) detail of juvenile

mesh at its proximal portion arrows show main uniseriate vein; (d) detail of proximal portion of adult mesh, arrow show polychotomous branching; (e) detail of early

stages of the mesh arrow sign rhizoidal elongation; (f) distal portion of the mesh showing decreasing perforations, arrow sign anastomosis of marginal cells and decrease of

preforation size.

Fig. A.2. Anadyomene stellata morphological characteristics. (a) Thallus habit; (b) view of eperforated blade, arrows sign uniseriate mid veins; (c) detail of proximal portion

of blade, arrow show polychotomous branching and swollen cells at their distal portion; (d) mid portion of the blade, arrow sign paralelle intersticial cells; (e) proximal

section of the blade, arrow sign rhizoid detail; (f) distal section of the blade showing blade lobulal margin, arrows sign mariginal oval cells.

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Please cite this article in press as: Collado-Vides, L., et al., A persistent bloom of Anadyomene J.V. Lamouroux (Anadyomenaceae, Chlorophyta) in

Biscayne Bay, Florida. Aquat. Bot. (2013), http://dx.doi.org/10.1016/j.aquabot.2013.06.010